The relationship between burden and caregiver’s sleep disturbances in dementia: a systematic review

ABSTRACT Caregivers of people living with dementia (PLwD) have a high burden degree that leads to health issues, including sleep. Objective: This study aimed to analyze the impacts of the caregiving burden on caregiver’s sleep disturbances. Methods: This systematic review involved a qualitative analysis of publications on Web of Science and Pubmed/Medline databases published between February 2018 and August 2022. Results: A total of 27 studies were identified and analyzed. Caregiver’s sleep presents impairments in sleep latency, sleep fragmentation, sleep duration, subjective sleep quality, daytime dysfunction, and insomnia. Caregiver’s distress and depressive symptoms have a dual relationship with sleep problems. Conclusion: Sleep disturbances presented by caregivers are correlated with higher burden levels and lead to more vulnerability to psychiatric symptoms and health issues.


INTRODUCTION
G lobal life expectancy increases every year and, with this, the number of people with dementia.Caregivers of people living with dementia (PLwD) are often relatives or close friends who spend one decade in the care 1 and, despite the disinformation about the symptoms, are mainly responsible for its management 2 , generally experiencing burden.The term "burden" refers to the impact that providing care for a family member has on a caregiver's life 3 .This population can experience impacts on mental, physical, emotional, and financial health 4 .Generally, burden has a mutual impact on sleep and high stress levels, leading to depression, anxiety, and poor sleep quality 5,6 .
Sleeping is crucial to maintain emotional and physical health, but nearly 63% of family caregivers are affected by chronic insomnia 7 , which predicts caregiver strain 1 .The sleep average of caregivers is 6.5 hours per night 8,9 , contrary to the recommendation of the National Sleep Foundation for older adults that determines 8 hours of sleep for optimal wellbeing 10 .The total hours of sleep are impacted by the nighttime care needed, leading to exhaustion the next day and daytime impairment 2,[11][12][13] .
Sleep disorders affect 50 to 70% of caregivers of PLwD 14 , resulting in long sleep onset latency, wake-after sleep onset, short sleep duration, low sleep efficiency 15,16 , changes in central stress, low sleep quality 17 , daytime sleepiness, poor self-rated sleep 18 , and sleep fragmentation 19 .These disturbances can negatively impact the immune system, elevate stress hormones, and increase the risk for cardiovascular diseases 20 , and the correlation between sleep and depressive symptoms predicts increased body mass index 21 , elevated coagulation, and inflammatory levels 22 .
This systematic review aimed to provide updated evidence on the relationship between caregivers' burden and sleep patterns.Specifically, the review focused on how caregiving impacts sleep quality and perceptions of sleep over the past five years.

METHODS
This systematic review was conducted following the methodology suggested by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRIS-MA) 23 .Literature research was carried out during January of 2023 using Web of Science and Pubmed/Medline databases.Search keywords were "Caregivers sleep AND Dementia," "Caregiver AND Sleep Problems," "Insomnia AND Caregivers," "Sleep Quality AND Dementia," "Sleep Quality AND Caregivers," "Sleep AND Caregivers," and "Dementia AND sleep." Inclusion criteria were: • cross-sectional and longitudinal, randomized and non-randomized studies; • studies with caregivers of PLwD; • studies that included sleep in the outcomes.

Exclusion criteria were:
• studies with etiologies other than dementia; • case reports; • meta-analyses and systematic reviews; and • studies with inpatients.
The authors read the selected abstracts and, when there was not enough information in the abstract to determine inclusion and exclusion criteria, the full text was retrieved.Two authors then independently reviewed the complete publications of the remaining papers and reached a consensus regarding inclusion criteria.The included studies were categorized according to their design, sample, method, and results.All selected articles were published between February 2018 and August 2022 and were in English.Data extraction occurred between February 2023 and April 2023.
To help analyze the quality of the articles found, the Mixed Methods Appraisal Tool (MMAT) 24 was used.MMAT is a tool that helps to identify the methodological quality of qualitative research, randomized controlled trials, non-randomized studies, quantitative descriptive studies, and mixed method studies.In the results table, every item evaluated in the analysis has a rate between 1 and 7.
Initial screening was performed by conferring the publication date and reading the title and abstracts.Articles that did not meet inclusion criteria were excluded, and those that were possibly eligible were retained, then read in entirety to confirm eligibility.The reasons for the article's exclusion were registered in the PRISMA flowchart (Figure 1).
Information collected through sleep and burden scales and objective measures of altered sleep patterns obtained through polysomnography and actigraphy were considered.Caregivers' characteristics were obtained from sixteen articles that specified gender, relationship with the care recipient, time spent on tasks, and age.
This systematic review was registered in the International Prospective Register of Systematic Reviews (PROSPERO) under CRD42023392955.

RESULTS
One hundred and four articles were found in the databases, and two registers were identified through Google Scholar.After removing duplicates, ninety-five articles were selected for the analysis according to inclusion criteria.Inclusion/exclusion criteria excluded seventy-two articles, remaining twenty-seven articles for final inclusion, with 19,859 caregivers analyzed.Table 1 depicts the study's main characteristics and results.
Three studies used the Insomnia Severity Index (ISI) 17,22,30 , leading to a need for more specific information about this disturbance.

Caregiver sleep quality scores
The PSQI is a highly used self-reported questionnaire that evaluates sleep quality over the past month.The validity of PSQI is considered good, with a specificity of 86.5% and a sensitivity of 89.6% 35  Generally, the studies that used the PSQI to evaluate sleep quality expressed a global score above 5 1,3- 5,11,14,21,25,31-33 .Only Liu et al. 34 found a global score below 5. Unfortunately, two studies did not show the total score of PSQI 18,27 .
The association between role burden and maintenance insomnia was found in one study 8 .Jiménez-Gonzalo et al. 17 found no correlation between caregiver sleep disturbances and significative scores on the ISI.
Differences in caregiver sleep according to dementia type Sleep disturbances are more prevalent in caregivers of individuals with neuropsychiatric symptoms, with caregivers presenting worse sleep quality when care recipients present disrupted behaviors 22 .More caregiving hours, a higher number of medical/nursing tasks, and more impairments in daily living implicate higher scores in the Level of Care Index (LCI), more sleep fragmentation, and greater sleep latency 14,18 .Also, recipients who presented sleep problems, such as difficulties in falling back asleep after waking up in the middle of the night, were associated with the caregiver having more sleep interruption 19 .
Recipients with Frontotemporal Dementia (FTD) and Dementia with Lewy Bodies (DLB) tend to present more neuropsychiatric symptoms demanding more care, leading to a higher burden and, consequently, more sleep problems 33 .Comparatively, DLB caregivers present more sleep problems than Alzheimer Disease (AD) caregivers.Other types of dementia were not analyzed 31 .

DISCUSSION
This systematic review aimed to analyze the relationship between burden and sleep disturbances in caregivers of PLwD.Recent studies have found that the most impaired sleep components were sleep latency (the time the person takes to fall asleep after going to bed) 1,5,18,26,33 and sleep fragmentation (sleep interruptions through the night) 13,18,19,26 .In addition, our findings corroborate the hypothesis that caregivers tend to spend less than seven hours in bed, leading to negative impacts on sleep quality and quantity, suggesting that this population has shorter sleep duration 3,18 , low subjective sleep quality 1,20 , maintenance insomnia 8 and low sleep efficiency 1,6 .
Caregivers' burden and distress positively correlate with sleep disturbances 5,11,15 .The perception of impairments in sleep quality is correlated with higher levels of burden 33 .Also, the daily stressor of caring for PLwD is related to reactivity in the hypothalamic-pituitary-adrenal (HPA) axis, leading to increased cortisol levels, which is related to less time in bed 12 .High cortisol levels negatively impact the Brain-Derived Neurotrophic Factor (BDNF), a neurotrophin related to sleep disorders 36 .The relationship between sleep and stress is mutual, once that the elevated rates of chronic stress 18 and its physiological changes can be responsible for alterations in sleep patterns.
Results suggest differences between types of dementia and caregivers' burden and sleep quality.For example, in FTD and DLB, the care recipient often presents agitation and sleep problems, which directly affects the quality of sleep and burden perception of caregivers 34 .Our findings also showed that caregivers who spend more hours caring for or performing more medical/nursing tasks have greater sleep fragmentation and latency 18 .
Sleep disorders are responsible for health problems such as high blood pressure 19 , higher Body Mass Index (BMI) 21 , high cortisol levels 12 , and psychiatric disorders 1 .Burden and sleep impairments often lead caregivers to present moderate depressive symptoms that lead to higher sleep latency, a greater number of wakes after sleeping, and low sleep efficiency 22,26,31 .
Cognitive impairments can be observed in this population 6 .For example, deficits in processing speed lead to negative impacts on care and generate problems such as errors in medication administration.Prolonged sleep deficits are associated to reduced clearance of Beta-amyloid and Thau 6 , leading to higher chances of developing cognitive impairment or dementia.
Sleep duration and fragmentation impact the coping strategies adopted by caregivers 18 and their quality of life 29 .The perception of incapacity to rest can lead to inappropriate behaviors with the PLwD 15 once the caregiver tends to lay their frustrations and irritability in the care recipient.
Female caregivers often report more mental health complaints and sleep problems.However, gender comparison is compromised by the fact that most caregivers are women, so this is a bias when comparing the groups.Also, most studies have fewer males in the sample, which can impact the results.Furthermore, caregivers of PLwD living in the community have more sleep deficits, leading to severe distress 2,5 , once that they usually cohabit with the care recipient 3 .
In conclusion, the results found positive correlations between caregivers' sleep disturbances and burden, cognitive deficits, vulnerability to dementias, psychiatric disorders, and physical problems such as higher blood pressure, obesity, and high cortisol levels, predicting more significant mortality.
Understanding the factors related to caregiver sleep is essential to provide more health care to these populations and increase the quality of care given to PLwD.A telephone-based behavioral activation protocol showed that improved sleep quality leads caregivers to have a more positive perspective, reduced stress levels, and to be more open to accepting the opinions of health professionals 14 .
Better understanding and development of more effective interventions can lead to fewer health problems in caregivers and improve the quality of care provided to PLwD.Also, understanding and helping caregivers to improve their sleep quality and consequently their quality of life can reduce government financial expenditure on health systems, as there will be a healthier population.

Figure 1 .
Figure 1.Flowchart of search and review process.

Table 1 .
Studies' main characteristics and results.
Abbreviations: AD, Alzheimer Disease; DLB, Dementia with Lewy Bodies; MCI, Mild Cognitive Impairment; PSQI, Pittsburgh Sleep Quality Index; ZBI, Zarit Burden Interview Short Version; GAD-7, Generalized Anxiety Disorder Scale; PHQ-9, Patient Health Questionnaire-9; CES-D, Center for Epidemiological Scale-Depression; PLwD, People Living with Dementia; DASS-21, Depression, Anxiety and Stress Scale; COPE-NVI, Coping Orientation to the Problems Experienced; HRQoL, Health-related Quality of Life; PSS, Perceived Stress Scale; EQ-5D, European Quality of Life Five Dimension; NPI, Neuropsychiatric Inventory; BPSD, Behavioral and Psychological Symptoms of Dementia; RSS, Relative Stress Scale; WCQ, Ways of Coping Questionnaire; CSES, Coping Self-Efficacy Scale; PMS, Personal Mastery Scale; PES-AD, Pleasant Events Schedule−AD; PANAS, Positive and Negative Affect Schedule; CESD-10, Center for Epidemiological Scale-Depression, 10 Item Version; LCI, Level of Care Index; HADS, Hospital Anxiety and Depression Scale; ISI, Insomnia Severity Index; POMS, Profile of Mood States; ICUB97-R, Data-gathering instrument based on Virginia Henderson's 14 Needs nursing model; PDD, Parkinson Disease Dementia; RMBPC, Revised Memory and Behavioral Problems Checklist; CGI, Marwit-Meuser Caregiver Grief Inventory; QoL, Quality of Life in Alzheimer Disease; PCI, The Perceived Change Index; PWB, Ryff Psychological Well-Being Scale; PHQ-2, Health Questionnaire 2-item Depression Scale; BDI-II, Beck Depression Inventory II; RSCSE, Revised Scale for Caregiving Self-Efficacy; BFI, Big Five Inventory; BRIEF-COPE, Self Report Questionnaire to Measure Cope Strategies in Stressful Life Events; SPM, Stress Process Model of Caregiving; CBI, Caregiver Burden Inventory SMI, SleepMed Insomnia Index.
. It analyzes seven sleep components that predict sleep quality: subjective sleep quality, sleep latency, sleep duration, sleep efficiency, sleep disturbances, use of sleep medication, and daytime dysfunction.A global score ≥5 predicts sleep disturbance.